"It is a characteristic of the design of scientific research that exquisite attention is devoted to methodological problems that can be solved, while the pretence is made that the ones that cannot be solved are really nothing to be worried about". 

[Richard Lewontin (2000). It ain't necessarily so: the dream of the human genome and other illusions. New York Review of Books, New York. p.237.]

I am going to worry about problems that cannot be solved, at least not for now. I will be concerned not so much with evolution of chlamydial pathogenicity as with evolution of chlamydiae themselves. What sort of beast was the last common ancestor (LCA) of the order Chlamydiales? Obligate intracellular parasites have appeared many times in the course of evolution. Why did the chlamydial LCA evolve into the extant representatives of the order instead of following other pathways to a totally different result? Just because there are no answers to these questions does not mean that they are not worth thinking about.

A general knowledge of chlamydial biology such as afforded by the monograph edited by Stephens (1999a) will be assumed and specific references will be limited to those directly concerned with the topics discussed.

There are four families in the order Chlamydiales (Everett et al., 1999; Rurangirwa et al., 1999; Everett, 2000). Two families are monogeneric and the other two have two genera each:

Table 1. The order Chlamydiales. Families, genera, species and true hosts

                      Taxon¹                                                      True hosts²

Chlamydiaceae
            Chlamydia
                     trachomatis                                                humans
                     suis                                                           pigs
                     muridarum                                                  mice, hamsters
            Chlamydophila
                     pneumoniae                                                humans, horses? koalas? frogs?
                     psittaci                                                       birds, muskrats, cattle
                     abortus                                                       ruminants
                     felis                                                            cats
                     caviae                                                         guinea pigs
                     pecorum                                                      ruminants, koalas?

Simkaniaceae
              Simkania
                     negevensis                                                  humans

Parachlamydiaceae
              Parachlamydia
                     acanthamoeba                                             amoebae
              Neochlamydia
                      hartmanellae                                               amoebae

Waddliaceae
              Waddlia
                      chondrophila                                               cattle

¹ The classification of Everett et al., (1999) is used.

² A true host is one that is infected in nature, supports multiplication of the pathogen, and releases its progeny to infect more individuals of the same host species (Woodhouse et al., 2001). 

Representatives of the order Chlamydiales have 16S rRNA sequences that are more than 80% identical and share phenotypic properties which I shall describe shortly. The last decade has seen a dramatic expansion in the known limits of the order. New families, genera, and species have been described, and new hosts have been discovered. Continued expansion is inevitable. 16S rRNA sequences have been recovered from humans and from free-living amoebas that group with Chlamydiales but cannot be placed within existing taxons. Intracellular organisms putatively identified as Chlamydiales have been identified in reptiles, amphibians, fish, arthropods, coelenterates, and mussels. Molecular confirmation is often lacking, but some of these organisms probably belong in Chlamydiales. New representatives of existing taxons must also be expected. The variety of Chlamydiales inhabiting amoebas seems almost unlimited. It is also unlikely that Simkaniaceae and Waddliaceae will long be represented by single species. Even Chlamydiaceae may hold some surprizes. By 1970, "psittacosis-lymphogranuloma-trachoma agents" had been identified in nearly every order of mammals and birds, almost always only by observation with the light microscope and transfer of infection into eggs and mice. What novel ribosomal RNA sequences might be recovered from some of these isolates from rarely studied hosts?

Broadened appreciation of the complexity of the taxon Chlamydiales gives free rein to speculation on evolutionary origins and pathways. However, looking at the evolution of the entire order, all four families at once, is made difficult by the disproportionally large amount of information on a single family, Chlamydiaceae, including complete genomes of representatives of both Chlamydia and Chlamydophila. For this reason, I will consider evolution of Chlamydiales in two parts. In the first, I will speculate on the evolution of the order as a whole, with my speculations limited by the information available. In the second, I will explore the evolutionary implications of the comparative wealth of information on Chlamydiaceae.